Protective effect of resveratrol on biomarkers of oxidative stress induced by iron/ascorbate in mouse spermatozoa

Nutrients

Volumn 6, Issue 2, 2014, Pages 489-503

  Mojica Villegas, María Angélica ^a   Izquierdo Vega, Jeannett Alejandra ^b   Chamorro Cevallos, Germán ^a   Sánchez Gutiérrez, Manuel ^b  

^a INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

^b University of the State of Hidalgo   (Mexico)

Author keywords

In vitro fertilization; Mitochondrial transmembrane potential; Oxidative stress; Resveratrol; Spermatozoa

Indexed keywords

ASCORBIC ACID; IRON; RESVERATROL; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CELL VIABILITY; ENZYME ACTIVITY; FEMALE; FERTILIZATION IN VITRO; LIPID PEROXIDATION; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; OXIDATIVE STRESS; PHASE CONTRAST MICROSCOPY; SEMEN ANALYSIS; SPERMATOZOON;

ANIMALS; ANTIOXIDANTS; ASCORBIC ACID; BIOLOGICAL MARKERS; FEMALE; GLUTATHIONE PEROXIDASE; LIPID PEROXIDATION; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SPERMATOZOA; STILBENES; SUPEROXIDE DISMUTASE; THIOBARBITURIC ACID REACTIVE SUBSTANCES;

EID: 84893305881     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu6020489     Document Type: Article

References (51)

1. Storey, K.B. Oxidative stress: Animal adaptations in nature. Braz. J. Med. Biol. Res. 1996, 29, 1715-1733.
2. Sanocka, D.; Kurpisz, M. Reactive oxygen species and sperm cells. Reprod. Biol. Endocrinol. 2004, 2, 1-7.
3. Bansal, A.K.; Bilaspuri, G.S. Impacts of oxidative stress and antioxidants on semen functions. Vet. Med. Int. 2011, 2011, doi:10.4061/2011/686137.
4. Kopers, A.J.; de luliis, G.N.; Finnie, J.M.; McLaughlin, E.A.; Aitken, R.J. Significance of mitochondrial reactive oxygen species in the generation of oxidative stress in spermatozoa. Endocr. Res. 2008, 93, 3199-3207.
5. Aitken, R.J.; Baker, M.A. Oxidative stress, sperm survival and fertility control. Mol. Cell. Endocrinol. 2006, 250, 66-69.
6. Agarwal, A.; Gupta, S.; Sikka, S. The role of free radicals and antioxidants in reproduction. Suresh Curr. Opin. Obstet. Gynecol. 2006, 18, 325-332.
7. Tremellen, K. Oxidative stress and male infertility a clinical perspective. Hum. Reprod. Update 2008, 14, 243-258.
8. Kovacic, P.; Somanathan, R. Multifaceted approach to resveratrol bioactivity: Focus on antioxidant action, cell signaling and safety. Oxid. Med. Cell. Longev. 2010, 3, 86-100.
9. Bhat, K.; Kosmeder, J., II; Pezzuto, J. Biological effects of resveratrol. Antioxid. Redox Signal. 2001, 3, 1041-1064.
10. Cottart, C.; Antoine, V.; Morizot, C.; Beaudeux, J. Resveratrol bioavailability and toxicity in humans. Mol. Nutr. Food Res. 2010, 54, 7-16.
11. Xia, E.; Den, G.; Guo, Y.; Li, H. Biological activities of polyphenols from grapes. Int. J. Mol. Sci. 2010, 11, 622-646.
12. Juan, M.E.; González-Pons, E.; Munuera, T.; Ballester, J.; Rodríguez-Gil, J.E.; Planas, J.M. Trans-resveratrol, a natural antioxidant from grapes, increases sperm output in healthy rats. J. Nutr. 2005, 135, 757-760.
13. Shin, S.; Hee, J.J.; Park, D.; Jang, M.J.; Choi, J.H.; Choi, B.H.; Joo, S.S.; Nahm, S.S.; Kim, J.; Kim, Y.B. Trans-resveratrol relaxes the corpus cavernosum ex vivo and enhances testosterone levels and sperm quality in vivo. Arch. Pharm. Res. 2008, 31, 83-87.
14. Revel, A.; Raanani, H.; Younglai, E.; Xu, J.; Han, R.; Savouret, J.F.; Casper, R.F. Resveratrol, a natural aryl hydrocarbon receptor antagonist, protects sperm from DNA damage and apoptosis caused by benzo(a)pyrene. Reprod. Toxicol. 2001, 15, 479-486.
15. Uguralp, S.; Mizrak, B.; Bay Karabulut, A. Resveratrol reduces ischemia reperfusion injury after experimental testicular torsion. Eur. J. Pediatr. Surg. 2005, 15, 114-119.
16. World Health Organization (WHO). Laboratory Manual for the Examination of Human Semen and Semen Cervical Mucus Interaction; Cambridge University Press: Cambridge, UK, 2010.
17. Buege, J.A.; Aust, S.D. Microsomal lipid peroxidation. Metheods Enzymol. 1978, 52, 302-310.
18. Aitken, R.J.; Curry, B.J. Redox regulation of human sperm function: From the physiological control of sperm capacitation to the etiology of infertility and DNA damage in the germ line. Antioxid. Redox Signal. 2011, 14, 367-381.
19. Ford, W.C. Regulation of sperm function by reactive oxygen species. Hum. Reprod. Update 2004, 10, 387-399.
20. Griveau, J.F.; Dumont, E.; Renard, P.; Callegari, J.P.; Le Lannou, D. Reactive oxygen species, lipid peroxidation and enzymatic defence systems in human spermatozoa. J. Reprod. Fertil. 1995, 103, 17-26.
21. Buffone, M.G.; Ijiri, T.W.; Cao, W.; Merdiushev, T.; Aghajanian, H.K.; Gerton, G.L. Heads or tails? Structural events and molecular mechanisms that promote mammalian sperm acrosomal exocytosis and motility. Mol. Reprod. Dev. 2012, 79, 4-18.
22. Lavranos, G.; Balla, M.; Tzortzopoulou, A.; Syriou, V.; Angelopoulou R. Investigating ROS sources in male infertility: A common end for numerous pathways. Reprod. Toxicol. 2012, 34, 298-307.
23. Agarwal, A.; Tamer, M.S. Role of sperm chromatin abnormalities and DNA damage in male infertility. Hum. Reprod. Update 2003, 9, 331-345.
24. Zini, A.; San Gabriel, M.; Baazeem, A. Antioxidants and sperm DNA damage: A clinical perspective. J. Assist. Reprod. Genet. 2009, 26, 427-432.
25. Zini, A.; Al-Hathal, N. Antioxidant therapy in male infertility: Fact or fiction? Asian J. Androl. 2011, 13, 374-381.
26. Lombardo, F.; Sansone, A.; Romanelli, F.; Paoli, D.; Gandini, L.; Lenzi A. The role of antioxidant therapy in the treatment of male infertility: An overview. Asian J. Androl. 2011, 13, 690-697.
27. Mínguez-Alarcón, L.; Mendiola, J.; López-Espín, J.J.; Sarabia-Cos, L.; Vivero-Salmerón, G.; Vioque, J.; Navarrete-Muñoz, E.M.; Torres-Cantero, A.M. Dietary intake of antioxidant nutrients is associated with semen quality in young university students. Hum. Reprod. 2012, 27, 2807-2814.
28. Zareba, P.; Colaci, D.S.; Afeiche, M.; Gaskins, A.J.; Jørgensen, N.; Mendiola, J.; Swan, S.H.; Chavarro, J.E. Semen quality in relation to antioxidant intake in a healthy male population. Fertil. Steril. 2013, 100, 1572-1579.
29. Afeiche, M. Williams, P.L.; Mendiola, J.; Gaskins, A.J.; Jørgensen, N.; Swan, S.H.; Chavarro, J.E. Dairy food intake in relation to semen quality and reproductive hormone levels among physically active young men. Hum. Reprod. 2013, 28, 2265-2275.
30. Ourique, G.M.; Finamor, I.A.; Saccol, E.M.; Riffel, A.P.; Pês, T.S.; Gutierrez, K.; Gonçalves, P.B.; Baldisserotto, B.; Pavanato, M.A.; Barreto, K.P. Resveratrol improves sperm motility, prevents lipid peroxidation and enhances antioxidant defences in the testes of hyperthyroid rats. Reprod. Toxicol. 2013, 37, 31-39.
31. Yuluǧ, E.; Türedi, S.; Alver, A.; Türedi, S.; Kahraman, C. Effects of resveratrol on methotrexate-induced testicular damage in rats. Sci. World J. 2013, 2013, doi:10.1155/2013/489659.
32. Goldberg, D.M.; Ng, E.; Yan, J.; Karumanchirí A.; Soleas, G.J.; Diamandis, E.P. Regional differences in resveratrol isomer concentrations of wines from various cultivars. J. Wine Res. 1996, 7, 13-24.
33. McMurtrey, K.D. Resveratrol in Wine. In Wine: Nutritional and Therapeutic Benefits; Watkins, T.R., Ed.; Oxford University Press: Oxford, UK, 1997; pp. 45-55.
34. Juan, M.E.; Vinardell, M.P.; Planas, J.M. The daily oral administration of high doses of trans-resveratrol to rats for 28 days is not harmful. J. Nutr. 2002, 132, 257-260.
35. Patel, K.R.; Scott, E.; Brown, V.A.; Gescher, A.J.; Steward, W.P.; Brown, K. Clinical trials of resveratrol. Ann. N. Y. Acad. Sci. 2011, 1215, 161-169.
36. Silva, E.C.; Cajueiro, J.F.; Silva, S.V.; Soares, P.C.; Guerra, M.M. Effect of antioxidants resveratrol and quercetin on in vitro evaluation of frozen ram sperm. Theriogenology 2012, 77, 1722-1726.
37. Aitken, R.J.; Jane, S.; Clarkson, S.; Fishel, S. Generation of reactive oxygen species, lipid peroxidation, and human sperm function. Biol. Reprod. 1989, 40, 183-197.
38. Martínez-Pastor, F.; Aisen, E.; Fernández-Santos, M.R.; Esteso, M.C.; Maroto-Morales, A.; García-Álvarez, O.; Garde, J.J. Reactive oxygen species generators affect quality parameters and apoptosis markers differently in red deer spermatozoa. Reproduction 2009, 137, 225-235.
39. Buettner, G.R.; Jurkiewicz, B.A. Catalytic metals, ascorbate and free radicals: Combinations to avoid. Radiat. Res. 1996, 145, 532-541.
40. Armstrong, J.S.; Rajasekaran, M.; Chamulitrat, W.; Gatti, P.; Hellstrom, W.J.; Sikka, S.C. Characterization of reactive oxygen species induced effects on human spermatozoa movement and energy metabolism. Free Radic. Biol. Med. 1999, 26, 869-880.
41. Leonard, S.S.; Xia, C.; Jiang, B.H.; Stinefelt, B.; Klandorf, H.; Harris, G.K.; Shi, X. Resveratrol scavenges reactive oxygen species and effects radical-induced cellular responses. Biochem. Biophys. Res. Commun. 2003, 309, 1017-1026.
42. Gravance, C.G.; Garner, D.L.; Miller, M.G.; Berger, T. Fluorescent probes and flow cytometry to assess rat sperm integrity and mitochondrial function. Reprod. Toxicol. 2001, 15, 5-10.
43. Van Ginkel, P.R.; Sareen, D.; Subramanian, L.; Walker, Q.; Darjatmoko, S.R.; Lindstrom, M.J.; Kulkarni, A.; Albert, D.M.; Polans, A.S. Resveratrol inhibits tumor growth of human neuroblastoma and mediates apoptosis by directly targeting mitochondria. Clin. Cancer Res. 2007, 13, 5162-5169.
44. Zini, R.; Morin, C.; Bertelli, A.; Bertelli, A.A.; Tillement, J.P. Effects of resveratrol on the rat brain respiratory chain. Drugs Exp. Clin. Res. 1999, 25, 87-97.
45. Collodel, G.; Federico, M.G.; Geminiani, M.; Martini, S.; Bonechi, C.; Rossi, C.; Figura, N. Effect of trans-resveratrol on induced oxidative stress in human sperm and in rat germinal cells. Reprod. Toxicol. 2011, 31, 239-246.
46. Berrougui, H.; Grenier, G.; Loued, S.; Drouin, G.; Khalil, A. A new insight into resveratrol as an atheroprotective compound: Inhibition of lipid peroxidation and enhancement of cholesterol efflux. Atherosclerosis 2009, 207, 420-427.
47. López-Vélez, M.; Martinez-Martinez, F.; Del Valle-Ribes, C. The study of phenolic compounds as natural antioxidants in wine. Crit. Rev. Food Sci. Nutr. 2003, 43, 233-244.
48. Visconti, P.E.; Ning, X.; Fornes, M.W.; Alvarez, J.G.; Stein, P.; Connors, S.A.; Kopf, G.S. Cholesterol efflux-mediated signal transduction in mammalian sperm: Cholesterol release signals an increase in protein tyrosine phosphorylation during mouse sperm capacitation. Dev. Boil. 1999, 214, 429-443.
49. Gray, J.E.; Starmer, J.; Lin, V.S.; Dickinson, B.C.; Magnuson, T. Mitochondrial hydrogen peroxide and defective cholesterol efflux prevent in vitro fertilization by cryopreserved inbred mouse sperm. Biol. Reprod. 2013, 89, 17.
50. Kwak, S.S.; Cheonga, S.A.; Jeona, Y.; Leeb, E.; Choic, K.C.; Jeungc, E.B.; Hyun, S.H. The effects of resveratrol on porcine oocyte in vitro maturation and subsequent embryonic development after parthenogenetic activation and in vitro fertilization. Theriogenology 2012, 78, 86-101.
51. Lee, K.; Wang, C.; Chaille, J.M.; Machaty, Z. Effect of resveratrol on the development of porcine embryos produced in vitro. J. Reprod. Dev. 2010, 56, 330-335.